Training surgeons to optimize communication and symptom management in patients with life-limiting conditions: systematic review

Abstract Background Surgeons routinely care for patients with life-limiting illness, requiring communication and symptom management skills supported by appropriate training. The objective of this study was to appraise and synthesize studies that assessed surgeon-directed training interventions that aimed to optimize communication and symptom management for patients with life-limiting illness. Methods A PRISMA-concordant systematic review was undertaken. MEDLINE, Embase, Allied and Complementary Medicine Database (AMED), and the Cochrane Central Register of Controlled Trials were searched from inception until October 2022 for studies reporting on the evaluation of surgeon-training interventions intending to improve surgeons’ communication or symptom management of patients with life-limiting disease. Data on the design, trainer and patient participants, and the intervention were extracted. Risk of bias was assessed. Results Of 7794 articles, 46 were included. Most studies employed a before–after approach (29 studies) and nine included control groups with five being randomized studies. General surgery was the most frequently included sub-specialty (22 studies). Trainers were described in 25 of 46 studies. Most training interventions aimed to improve communication skills (45 studies) and 13 different training interventions were described. Eight studies reported a measurable improvement in patient care, such as increased documentation of advance care discussions. Most study outcomes focused on surgeons’ knowledge (12 studies), skills (21 studies), and confidence/comfort (18 studies) in palliative communication skills. Studies had a high risk of bias. Conclusion Whilst interventions exist to improve the training of surgeons managing patients with life-threatening conditions, evidence is limited, and studies measure the direct impact on patient care insufficiently. Improved research is needed to lead to better methods for training surgeons to benefit patients.


Introduction
Surgeons have critical decisions to make about patients' care that frequently balance the risk of death or disability with potential cure or alleviation of symptom burden. In a study of surgical patients receiving high-risk surgical procedures in the USA, between 15.2 and 24.0 per cent of patients died within 90 days of their procedure 1 . Reports from the USA show that up to one-third of elderly Medicare beneficiaries have an inpatient surgical procedure during their final year of life 2 . Meanwhile, one in five surgical inpatients in the UK is in their last year of life 3 . The Lancet Commission on the Value of Death highlights the overmedicalization of those reaching the end of their life, characterized by aggressive treatments and unnecessary suffering. It recommends improved death literacy for surgeons, among other health professionals, as an essential step to rebalancing the care of patients with life-threatening or life-limiting illness 4 . Symptom management and shared decision-making are key to end-of-life care.
Quality shared decision-making in surgery is associated with greater patient satisfaction, increased patient knowledge, and reduced anxiety 5 . Surgical best-practice guidelines in the UK and USA emphasize the importance of generalist palliative care skills in communication with and care of patients who are seriously ill [6][7][8] . These generalist palliative care skills include both palliative communication skills and skills in symptom management. There is a wealth of literature indicating improved patient and carer outcomes with the involvement of palliative care in the care of patients with life-limiting and life-threatening disease 1,9,10 . Therefore, it is unsurprising that there has been a growing recognition of the importance of palliative care training for surgeons, which has increased in the USA from 16 per cent (2005) to 80 per cent (2018) 11,12 . There are several different methods for training surgeons to achieve improved palliative care skills and shared decision-making, although it is uncertain which is most effective for patient benefit 13 . This study appraised and synthesized studies that assessed surgeon-directed training interventions that aimed to optimize communication and symptom management for patients with life-threatening illness (palliative care skills). The objective of this study was to describe the training interventions and evaluate the outcome measures used in these studies, particularly the use of patient-related outcomes, and understand the efficacy of these studies with relation to outcome measures, including surgeon confidence, knowledge, skill, and comfort.

Methods
The systematic review was conducted in accordance with PRISMA guidelines 14 and registered with the International Prospective Register of Systematic Reviews (CRD42020207532).

Search strategy
OVID SP versions of MEDLINE, Embase, Allied and Complementary Medicine Database (AMED), and the Cochrane Central Register of Controlled Trials were interrogated from time of inception until August 2020, with the search updated in October 2022. The search strategy used a combination of medical subject headings (MeSH) and free-text terms to identify papers that described surgeon-training interventions as below. The search strategy was developed by a palliative care physician (C.C.), surgeon (J.M.B.), and junior doctor (B.E.Z.) with advice from a medical librarian (Appendix S1). The search was supplemented by interrogation of reference lists of included studies. Relevant reviews and meta-analyses were screened for studies of interest.

Included studies
Two reviewers independently undertook study identification through title and abstract screening. Included papers are those that described the evaluation of surgeon-training interventions, defined as any intervention intending to improve surgeons' communication or symptom management of patients with severe, life-threatening, or life-limiting disease. Included in this study are mixed-population studies where surgeons were explicitly stated to be included. Key terms were used to identify palliative care focus in studies for inclusion. These included: palliative care, prognosis, goal orientated, goal concordant, advance care plan (ACP), end of life (EoL), serious illness, life-limiting illness, life-threatening, terminal care, and 'breaking bad news'. Intervention studies that reported the development of an intervention but did not assess its impact (that is that did not report clinician or patient outcomes) were excluded. Disagreements were resolved by discussion with the third reviewer/senior author. Eligible study designs included: RCTs, before-after studies, correlational studies, studies utilizing a single-arm experimental design, and quality improvement projects. Non-interventional studies, studies with insufficient primary data (opinion pieces, congress abstracts), qualitative studies, and non-English language studies were excluded. Where studies included some embedded qualitative analysis, qualitative results were not included in the narrative synthesis. Studies that focused on generic communication skills without any palliative care content were excluded. In addition, studies conducted with paediatric/obstetric surgeons were excluded due to the inherent difference in the surgeon-patient interactions.

Data extraction
Data extraction was undertaken by two reviewers independently. Data were recorded electronically in an Excel spreadsheet. Data relating to a description of the study included: author, year of publication, journal, study design, funding source, and the country in which the study took place. Data relating to the description of the intervention included: clinician inclusion and exclusion criteria, the sub-specialty of surgeons, patient characteristics, the number and discipline of educators/trainers, content and focus of the intervention (communication and/or symptom management), and the intervention training approach, including the number of approaches used. The results of intervention evaluation that pertained to clinician outcomes (such as change in knowledge or confidence) or patient impact (such as documentation of Do Not Attempt Cardiopulmonary Resuscitation (DNACPR) for patients treated by surgeons who had received the palliative training intervention) were extracted.

Quality assessment
The quality of reporting of all included studies was assessed using the Evidence Project risk-of-bias tool by two reviewers independently 15 . This tool was chosen due to its applicability to a range of study designs. Studies are not given a summary score of bias, but areas of significant bias within studies are highlighted.

Analysis
Studies were analysed first according to the focus of the intervention (communication or symptom management) and second according to the intervention outcome: outcomes, termed in this paper as 'patient outcomes,' that reflected quality of patient care, such as patient experience surveys, documentation of advance care planning discussions, or length of hospital stay; or studies that focused on surgeon benefit (self-assessed or externally assessed), such as the clinicians' perceived value of the intervention (confidence, knowledge, and self-reported practice) or objectively perceived changes in communication skills (Table S1).
A narrative account of interventions to improve essential generalist palliative care skills in surgeons was created using the framework described by Popay et al. 16 . A theory of how the intervention may have worked for surgeons was discussed and a preliminary synthesis of findings prepared and discussed with the research team. The robustness of the synthesis was tested by comparing the findings against relationships within the data.

Results of the search
Of 7794 screened articles, 46 were included in the final analyses ( Fig. 1) 13,17-61 .

Study description
Most studies employed a before-after approach (29 studies). Nine studies included control arms, of which five were RCTs. Five studies employed a single-arm experimental design. Two studies utilized an interrupted time-series design. Most studies took place in the USA (34 studies), four took place in Canada, three took place in Japan, two took place in Israel, two took place in Belgium, and one took place in Pakistan (Table S1).

Intervention description
The reported detail of the training intervention varied between studies. Studies involved between three and 345 surgeons (median = 31). Two studies included fewer than ten surgeons 21,48 . One was a teaching programme for juniors rotating through an intensive care unit (ICU), including three surgeons. The other, including eight surgeons, was a pilot of a grand round and objective structured clinical examination (OSCE) of leading a family conference in an ICU. Thirty studies described the surgeons' specialties. Frequently included specialties were general surgery (22 studies), gynaecology (6 studies), cardiothoracics (5 studies), and orthopaedics (5 studies). Fifteen of the included studies were mixed groups of surgeons and non-surgical clinicians.
The focus and therefore the content of the training interventions varied. Study focus included a focus on improving knowledge, skills, and/or behaviour. Some studies aimed to deliver all three aims, for instance, addressing communication knowledge and skills by supporting patients to describe their advance care wishes (advance directives/advance decision to refuse treatment (ADRT)) and having these appropriately documented.
Between one and six patient-specific care measures were included per study with significant inter-study heterogeneity. The most common patient care outcome was documentation of code or resuscitation status, advance directives/ADRT, or goals-of-care (GOC) conversations. Other outcomes included: the number of patients who received surgery, were admitted to ICU, received a palliative care consultation, the patient discharge destination 40 , length of hospital stay (for those patients needing ICU care) 28,59 , pain assessment (based on a notes review) 37 , patient-reported frequency with which doctors provided understandable information 43 , ventilator days, mortality rate, disposition, and frequency of invasive procedures 58,59 . Eight studies reported improvements in some patient care outcomes associated with the intervention. These included: increased likelihood that a physician had a GOC discussion 46  Titles and abstracts screened n = 6610 Full-text screened n = 245 Articles included from screening n = 39 Articles included n = 46 Articles included from snowball search n = 7 Abstracts excluded n = 6365 Duplicates excluded n = 1184 decreased non-beneficial care in an ICU setting 28 , increased patient rating of doctors' ability to provide understandable explanations 43 , improved shared decision-making 40 and improved pain scores of patients treated by surgeons who had undertaken a rotation in palliative care 37 , and a decrease in palliative care consultation 59 . Several studies described no improvement in specific patient outcomes related to palliative care training interventions. Amen et al. 59 implemented a 4-week multi-modal training programme for residents rotating through the surgical ICU and found an increase in ACP documentation and a reduction in ICU length of stay. However, they noted no change in mortality rate or the percentage of patients discharged in a persistent vegetative state 59 . A further study found no difference in the intensity of received treatment between patient groups pre-and post-intervention where trauma Attendings received training regarding the 'best case/worse case' (BC/WC) framework 58 , a communication approach to help support surgeons have goal-orientated patient consultations.
Taylor et al. 40 also evaluated the introduction of the BC/WC framework. This approach demonstrated mixed findings. There was improved shared decision-making using the OPTION 5 score (an observer measure of shared decision-making based on a 100 point scale) with an improvement in median score from 41 pre-intervention to 74 after training (intraclass correlation was 0.80 (95 per cent c.i. 0.64 to 0.90)). Patients seen by surgeons after the training intervention more frequently received the proposed surgery (42 per cent before the intervention versus 50 per cent after the intervention). However, patients seen by surgeons after the intervention were less frequently discharged home (50 per cent before the intervention versus 20 per cent after the intervention) or to a hospice (17 per cent before the intervention versus 5 per cent after the intervention) and were more frequently discharged to skilled nursing facilities (25 per cent before the intervention versus 45 per cent after the intervention)-although the intention of discharge (for example rehabilitation) was not stated.
Heterogeneous outcomes included: clinician perceived value of the intervention (25 studies), objectively assessed communication skills-assessed by a mixture of faculty, family, patients, or simulated patients (21 studies), self-assessed confidence, comfort, or competence (18 studies), objectively assessed knowledge (12 studies), self-reported practice improvement (7 studies), patient outcomes (7 studies), and 'other' (17 studies)-including perception of palliative care (measured by questionnaire), reported difficulties in practice, and participant attitudes regarding physician-patient communication.

Communication skills
Of the 21 19 39,53,57,61 . Three of these found that an intensive communication skill training course significantly improved the palliative communication skills of clinicians 53,57,61 . One study compared an intervention group with a comparison group post-intervention, but not to baseline scores-this study found no difference between groups 19 . Of eight 26,27,30,33,40,43,56,58 studies using a before-after design with no control group, six showed significant improvement after the intervention 26,30,40,43,56,59 compared with clinicians' baseline scores. Risk of bias was generally high across these studies due to the paucity of studies utilizing control groups and the poor follow-up rates of the before-after studies, of which only three had a follow-up rate of greater than or equal to 80 per cent 27,30,40 . Self-reported confidence, comfort, or competence Clinicians' self-assessed confidence, comfort, or competence relating to communication skills was recorded in 18 studies. Only one study 34 included pre-and post-intervention tests and a comparison group to examine self-assessed confidence, comfort, or competence in generalist palliative communication skills. This study showed no difference between intervention and control groups. One study used a control group and post-pre assessment, with retrospective assessment occurring at the time of post-intervention assessment. This study showed significant improvement in the intervention group, but did not report the results of the control group 61 . Sixteen 13,17,19,20,24,31,33,35,36,[42][43][44]47,48,51,60 studies tested this outcome measure using pre-and post-intervention tests (without a comparison group); of these, 11 13,17,24,31,35,36,42,43,47,48,60 showed increased self-reported confidence, comfort, or competence measures. However, the lack of control groups used in the evaluation of this outcome measure is indicative of a high risk of bias in these results.

Self-reported practice
Study clinician-participants' self-reported practice improved across all seven 20,29,36,41,49,50,54 studies that measured this outcome, with one study showing this compared with a control group 29 and another reporting sustained improvement 6 months post-intervention 20 . However, the evaluation of this outcome is at risk of bias due to the few control groups used in its evaluation.

Description of symptom management studies
Among the seven 19,29,34,37,38,54,55 studies investigating palliative symptom management, six measured knowledge acquisition 19,29,34,38,54,55 . All six studies showed that some knowledge domains (for example management of cancer pain, opioid side effects, delirium, and symptom markers of poor end-of-life care) improved after the training intervention. Only two of these showed improvement compared with a control group 29,34 . Three 19,34,37 of the seven symptom management studies measured self-assessed confidence, of which one compared this with a control group 34 , and all showed improvement associated with the intervention. However, the lack of control groups in most studies suggests a high risk of bias in these studies. Both studies that reported on self-reported practice relating to care of the dying patient (including pain and dyspnoea) found an improvement in self-reported practice scores after the intervention, with only one showing this compared with a control group 29,54 .

Quality assessment
The Evidence Project risk-of-bias tool checklist is presented in Table S2. Twenty-two studies reached the Evidence Project risk-of-bias tool predefined follow-up rate of 80 per cent in at least one domain (for example in the knowledge test). Forty-five studies did not select clinician-participants randomly for assessment.

Discussion
This systematic review found 46 studies evaluating surgeon-directed palliative care training. Of these, nine studies measured the impact of surgeon-directed training on patient care outcomes, with eight showing improvement in some patient care outcome measures, such as shared decision-making. Of these nine studies, three were published since 2021. The remainder focused on benefits to surgeons. Overall, included studies showed that surgeons' skill, knowledge, confidence, and comfort with palliative communication and symptom management improved after the training interventions. However, the subjective nature of some outcomes, such as self-perceived confidence and comfort, and the frequent absence of control groups, limits the extent to which they can be considered evidence for the success of an intervention. This is especially true given the conflicting literature on the relationship between clinicians' confidence and competence 62,63 . Therefore, while there is some mixed evidence that surgeon-directed palliative care training improves patient care and perceived knowledge and skills amongst surgeons, the latter cannot be extrapolated to demonstrate sustained improvement in patient care conclusively. This emphasizes the need for more research in this area.
This review echoes concerns raised in a 2017 systematic review around training surgeons and anaesthesiologists in end-of-life conversations, describing flawed study methodology, such as an absence of control groups, and inadequate patient outcome measures 64 . Compared with previous reviews, the current review has identified some progress in the field, with studies that report specifically on communication in the perioperative interval 40 and communication of poor prognosis and unexpected death in the trauma bay 51 , which previously has been found lacking 65 .
It has been suggested that surgeons have reduced responsiveness to emotional cues and increased focus on medical details 66,67 . However, whether training surgeons to redress the balance to have more effective goal-concordant discussions is the most effective means to improve outcomes for patients with life-limiting illness in surgical settings is not known. There is evidence that multidisciplinary working between surgeons, palliative care physicians, and geriatricians is associated with reduced length of stay, healthcare costs, and mortality rate 68,69 . However, there is no evidence comparing training surgeons in palliative care skills with other organizational levers that increase multidisciplinary working in the perioperative interval.
Surgical referrals to specialist palliative care have increased over time. This is attributed to the introduction of greater palliative care exposure in training and a culture change stemming from publications, such as the American College of Surgeons' Statement of Principles of Palliative Care 12 , and the UK Royal College of Surgeons' Caring for Patients Nearing the End of Life 6 . However, a number of studies still describe inadequate inclusion of palliative care in surgical curricula and identify gaps in surgical training around end-of-life conversations and prognostication in particular; therefore, this review is timely and important [21][22][23] .
The strengths of this review include the completeness of the search strategy and inclusion criteria. No other systematic review in the field has included interventional studies aimed at improving palliative communication skills and symptom management for surgeons. The internal validity of this review was strengthened by dual and independent abstract screening, full-text screening, data extraction, and quality assessment. A limitation is the non-inclusion of studies reporting on the development of training interventions, as key interventions may consequently have been missed. Non-controlled studies were included in this study due to the frequency of surgeon perception, experience, or change in practice as a study outcome measure.
A limitation of the data is the inability to carry out a meta-analysis due to the heterogeneity of interventions, outcome measures, and methods of evaluation. Unfortunately, the range of multi-modal intervention approaches, combined with a variety of outcome measures, mean it is impossible to identify the most effective training intervention.
The measurement of patient care as an assessment of training quality is becoming more widespread 70,71 . It is clear this evolution would also benefit studies of surgical postgraduate training. Many of the included studies that addressed patient care outcomes relied on routine data, such as length of stay, or documentation of GOC discussions. The greater use of patient experience and palliative care-specific outcome measures, such as the palliative care outcome scale (POS) 72 , which consider the physical, psychosocial, and spiritual domains of care quality, would be beneficial.
Important and recurring limitations of included studies included single-centre, small sample-size studies with unvalidated, non-systematic outcome assessment that did not account for a maturation effect or sustained change over time.
Other important limitations to note are the infrequency with which control or comparison groups were used, the lack of randomization, and the paucity of studies reporting patient outcomes. All of these limitations are common in the literature around the effectiveness of postgraduate training interventions 73 .
This study varied from the published protocol in the exclusion of studies reporting on anaesthetists and intensivists as a participant population in the absence of surgical participants. This was due to the large number of studies retrieved and the consequent difficulty in synthesizing and comparing results. In addition, qualitative results were not included due to the significant heterogeneity in methods utilized and outcomes measured.
Future research in postgraduate palliative care training would benefit from universally agreed patient outcome measures. While the use of surrogate outcomes in training interventions, such as clinician confidence or clinician-perceived value of the intervention, has advantages (reduced cost, simpler and less time-consuming ethical approval), their continued use requires demonstration that they reflect a pathway to improved patient care. Reporting of postgraduate training interventions can be improved using a bespoke statement, such as the guideline for reporting evidence-based practice educational interventions and teaching (GREET) statement 74 or the criteria for describing and evaluating training interventions in healthcare professions (CRE-DEPTH) 75 . Although the GREET statement is not specific to palliative care postgraduate training, its use would significantly improve reporting, and, where consulted at intervention development, would likely improve the quality of studies performed 76 . Finally, underlying epidemiological principles clearly point to the need to improve intervention design with the use of randomization and control arms for training interventions and systematic outcome reporting methods.
This study provides the most complete overview of attempts to improve palliative care skills in surgeons to date. Palliative care training interventions objectively and subjectively improve surgeons' assessed skill, knowledge, and confidence in palliative communication and symptom management. Nevertheless, there is insufficient focus on patient outcomes as evidence of the impact of palliative care training, and heterogeneity of patient outcome measures confounds synthesis of the study findings. However, of the studies published since 2021, three of five studies included use of patient outcome measures, indicating potential progress in this field of research. Greater implementation of standardized reporting statements in studies of postgraduate palliative care training would improve the conduct and reporting of research in this field.

Funding
This study was supported by the NIHR Biomedical Research Centre at University Hospitals Bristol and Weston NHS Foundation Trust and the University of Bristol.